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The Korean Society of Phycology (한국조류학회(藻類))
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Physiological effects of copper on the freshwater alga Closterium ehrenbergii Meneghini (Conjugatophyceae) and its potential use in toxicity assessments

  • Received : 2017.02.02
  • Accepted : 2017.05.24
  • Published : 2017.06.15
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Abstract

Although green algae of the genus Closterium are considered ideal models for testing toxicity in aquatic ecosystems, little data about the effects of toxicity on these algal species is currently available. Here, Closterium ehrenbergii was used to assess the acute toxicity of copper (Cu). The median effective concentration ($EC_{50}$) of copper sulfate based on a dose response curve was $0.202mg\;L^{-1}$, and reductions in photosynthetic efficiency ($F_v/F_m$ ratio) of cells were observed in cultures exposed to Cu for 6 h, with efficiency significantly reduced after 48 h (p < 0.01). In addition, production of reactive oxygen species significantly increased over time (p < 0.01), leading to damage to intracellular organelles. Our results indicate that Cu induces oxidative stress in cellular metabolic processes and causes severe physiological damage within C. ehrenbergii cells, and even cell death; moreover, they clearly suggest that C. ehrenbergii represents a potentially powerful test model for use in aquatic toxicity assessments.

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References

  1. Anton, F. A., Laborda, E. & Laborda, P. 1993. Acute toxicity of technical captan to algae and fish. Bull. Environ. Contam. Toxicol. 50:392-399.
  2. Cairns, J., Buikema, A. L., Heath, A. G. & Parker, B. C. 1978. Effects of temperature on aquatic organism sensitivity to selected chemicals. Bulletin 106. Virginia Water Resources Research Center, Blacksburg, VA, 88 pp.
  3. Chen, H., Chen, J., Guo, Y., Wen, Y., Liu, J. & Liu, W. 2012. Evaluation of the role of the glutathione redox cycle in Cu (II) toxicity to green algae by a chiral perturbation approach. Aquat. Toxicol. 120-121:19-26. https://doi.org/10.1016/j.aquatox.2012.04.011
  4. Ebenezer, V. & Ki, J. -S. 2013. Quantification of the sub-lethal toxicity of metals and endocrine-disrupting chemicals to the marine green microalga Tetraselmis suecica. Fish. Aquat. Sci. 16:187-194.
  5. Ebenezer, V., Lim, W. A. & Ki, J. -S. 2014. Effects of the algicides $CuSO_4$ and NaOCl on various physiological parameters in the harmful dinoflagellate Cochlodinium polykrikoides. J. Appl. Phycol. 26:2357-2365. https://doi.org/10.1007/s10811-014-0267-9
  6. Ferrat, L., Pergent-Martini, C. & Romeo, M. 2003. Assessment of the use of biomarkers in aquatic plants for the evaluation of environmental quality: application to seagrasses. Aquat. Toxicol. 65:187-204. https://doi.org/10.1016/S0166-445X(03)00133-4
  7. Franklin, N. M., Stauber, J. L., Apte, S. C. & Lim, R. P. 2002. Effect of initial cell density on the bioavailability and toxicity of copper in microalgal bioassays. Environ. Toxicol. Chem. 21:742-751. https://doi.org/10.1002/etc.5620210409
  8. Fukumoto, R. -H., Fujii, T. & Sekimoto, H. 1997. Detection and evaluation of a novel sexual pheromone that induces sexual cell division of Closterium ehrenbergii (Chlorophyta). J. Phycol. 33:441-445. https://doi.org/10.1111/j.0022-3646.1997.00441.x
  9. Giardi, M. T., Koblizek, M. & Masojidek, J. 2001. Photosystem II-based biosensors for the detection of pollutants. Biosens. Bioelectron. 16:1027-1033. https://doi.org/10.1016/S0956-5663(01)00197-X
  10. Guo, R., Ebenezer, V. & Ki, J. -S. 2014. PmMGST3, a novel microsomal glutathione S-transferase gene in the dinoflagellate Prorocentrum minimum, is a potential biomarker of oxidative stress. Gene 546:378-385. https://doi.org/10.1016/j.gene.2014.05.046
  11. Guo, R., Lim, W. -A. & Ki, J. -S. 2016a. Genome-wide analysis of transcription and photosynthesis inhibition in the harmful dinoflagellate Prorocentrum minimum in response to the biocide copper sulfate. Harmful Algae 57:27-38. https://doi.org/10.1016/j.hal.2016.05.004
  12. Guo, R., Wang, H., Suh, Y. S. & Ki, J. -S. 2016b. Transcriptomic profiles reveal the genome-wide responses of the harmful dinoflagellate Cochlodinium polykrikoides when exposed to the algicide copper sulfate. BMC Genomics 17:29. https://doi.org/10.1186/s12864-015-2341-3
  13. Ichimura, T. & Kasai, F. 1984. Post-zygotic isolation between allopatric mating groups of Closterium ehrenbergii Meneghini (Conjugatophyceae). Phycologia 23:77-85. https://doi.org/10.2216/i0031-8884-23-1-77.1
  14. Ishikawa, T., Takeda, T., Shigeoka, S., Hirayama, O. & Mitsunaga, T. 1993. Hydrogen peroxide generation in organelles of Euglena gracilis. Phytochemistry 33:1297-1299. https://doi.org/10.1016/0031-9422(93)85078-6
  15. Juneau, P., Sumitomo, H., Matsui, S., Itoh, S., Kim, S. -G. & Popovic, R. 2003. Use of chlorophyll fluorescence of Closterium ehrenbergii and Lemna gibba for toxic effect evaluation of sewage treatment plant effluent and its hydrophobic components. Ecotoxicol. Environ. Saf. 55:1-8. https://doi.org/10.1016/S0147-6513(02)00130-6
  16. Kim, J. -D., Kim, B. & Lee, C. -G. 2007. Alga-lytic activity of Pseudomonas fluorescens against the red tide causing marine alga Heterosigma akashiwo (Raphidophyceae). Biol. Control 41:296-303. https://doi.org/10.1016/j.biocontrol.2007.02.010
  17. Kim, S. -G., Matsui, S. & Hamada, J. 1998. Toxicity test of anionic and nonionic surfactants to Closterium ehrenbergii by new indexes. J. Environ. Conserv. Eng. 27:274-281. https://doi.org/10.5956/jriet.27.274
  18. Knauert, S. & Knauer, K. 2008. The role of reactive oxygen species in copper toxicity to two freshwater green algae. J. Phycol. 44:311-319. https://doi.org/10.1111/j.1529-8817.2008.00471.x
  19. Lee, M. -A., Guo, R., Ebenezer, V. & Ki, J. -S. 2015. Evaluation and selection of reference genes for ecotoxicogenomic study of the green alga Closterium ehrenbergii using quantitative real-time PCR. Ecotoxicology 24:863-872. https://doi.org/10.1007/s10646-015-1430-z
  20. Lee, M. -A., Guo, R. & Ki, J. -S. 2014. Different transcriptional responses of heat shock protein 20 in the marine diatom Ditylum brightwellii exposed to metals and endocrine-disrupting chemicals. Environ. Toxicol. 29:1379-1389. https://doi.org/10.1002/tox.21868
  21. Lewis, M. A. 1995. Algae and vascular plant tests. In Rand, G. M. (Ed.) Fundamentals of Aquatic Toxicology: Effects, Environmental Fate, and Risk Assessment. Taylor and Francis, Washington, DC, pp. 135-169.
  22. Li, X., Ping, X., Xiumei, S., Zhenbin, W. & Liqiang, X. 2005. Toxicity of cypermethrin on growth, pigments, and superoxide dismutase of Scenedesmus obliquus. Ecotoxicol. Environ. Saf. 60:188-192. https://doi.org/10.1016/j.ecoenv.2004.01.012
  23. Magdaleno, A., Velez, C. G., Wenzel, M. T. & Tell, G. 2013. Effects of cadmium, copper and zinc on growth of four isolated algae from a highly polluted Argentina river. Bull. Environ. Contam. Toxicol. 92:202-207.
  24. Mamboya, F. A., Pratap, H. B., Mtolera, M. & Bjork, M. 1999. The effect of copper on the daily growth rate and photosynthetic efficiency of the brown macroalga Padina boergesenii. In Richmond, M. D. & Francis, J. (Eds.) Proceedings of the 20th Anniversary Conference on Advances on Marine Sciences in Tanzania, IMS/WIOMSA, Zanzibar, pp. 185-192.
  25. Manimaran, K., Karthikeyan, P., Ashokkumar, S., Ashok Prabu, V. & Sampathkumar, P. 2012. Effect of copper on growth and enzyme activities of marine diatom, Odontella mobiliensis. Bull. Environ. Contam. Toxicol. 88:30-37. https://doi.org/10.1007/s00128-011-0427-4
  26. OECD. 2006. OECD guidelines for the testing of chemicals. Test No. 201. Freshwater algal and cyanobacteria, growth inhibition test. OECD Publications, Paris, 25 pp.
  27. Qian, H., Chen, W., Sheng, G. D., Xu, X., Liu, W. & Fu, Z. 2008. Effects of glufosinate on antioxidant enzymes, subcellular structure, and gene expression in the unicellular green alga Chlorella vulgaris. Aquat. Toxicol. 88:301-307. https://doi.org/10.1016/j.aquatox.2008.05.009
  28. Qin, Y., Lu, M. & Gong, X. 2008. Dihydrorhodamine 123 is superior to 2,7-dichlorodihydrofluorescein diacetate and dihydrorhodamine 6G in detecting intracellular hydrogen peroxide in tumor cells. Cell Biol. Int. 32:224-228. https://doi.org/10.1016/j.cellbi.2007.08.028
  29. Sabatini, S. E., Juarez, A. B., Eppis, M. R., Bianchi, L., Luquet, C. M. & Rios de Molinaa, M. C. 2009. Oxidative stress and antioxidant defences in two green microalgae exposed to copper. Ecotoxicol. Environ. Saf. 72:1200-1206. https://doi.org/10.1016/j.ecoenv.2009.01.003
  30. Sathasivam, R., Ebenezer, V., Guo, R. & Ki, J. -S. 2016. Physiological and biochemical responses of the freshwater green algae Closterium ehrenbergii to the common disinfectant chlorine. Ecotoxicol. Environ. Saf. 133:501-508. https://doi.org/10.1016/j.ecoenv.2016.08.004
  31. Sato, M., Murata, Y., Mizusawa, M., Iwahashi, H. & Oka, S. -I. 2004. A simple and rapid dual-fluorescence viability assay for microalgae. Microbiol. Cult. Coll. 20:53-59.
  32. Sbihi, K., Cherifi, O., El gharmali, A., Oudra, B. & Aziz, F. 2012. Accumulation and toxicological effects of cadmium, copper and zinc on the growth and photosynthesis of the freshwater diatom Planothidium lanceolatum (Brébisson) Lange-Bertalot: a laboratory study. J. Mater. Environ. Sci. 3:497-506.
  33. Schreiber, U., Hormann, H., Neubauer, C. & Klughammer, C. 1995. Assessment of photosystem II photochemical quantum yield by chlorophyll fluorescence quenching analysis. Aust. J. Plant Physiol. 22:209-220. https://doi.org/10.1071/PP9950209
  34. Trampe, E., Kolbowski, J., Schreiber, U. & Kuhl, M. 2011. Rapid assessment of different oxygenic phototrophs and single-cell photosynthesis with multicolour variable chlorophyll fluorescence imaging. Mar. Biol. 158:1667-1675. https://doi.org/10.1007/s00227-011-1663-1
  35. U.S. Environmental Protection Agency. 1986. Environmental standards. General standards: General standards for discharge of environmental pollutant. Available from: http://ercmp.nic.in/Documents/GenEnvStandard.pdf. Accessed Apr 2, 2017.
  36. Viana, S. M. & Rocha, O. 2005. The toxicity of copper sulphate and atrazine to the diatom Aulacoseira Granulata (Ehrenberg) Simmons. Acta Limnol. Bras. 17:291-300.
  37. Watanabe, M. M., Kawachi, M., Hiroki, M. & Kasai, F. 2000. NIES collection list of strains. 6th ed. 2000 microalgae and protozoa. Microbial Culture Collections, National Institute for Environmental Studies, Tsukuba, 159 pp.
  38. Young, R. G. & Lisk, D. J. 1972. Effect of copper and silver ions on algae. J. Water Pollut. Control Fed. 44:1643-1647.

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